@article{GechevBeninaObataetal.2013,
  author    = {Gechev, Tsanko S. and Benina, Maria and Obata, Toshihiro and Tohge, Takayuki and Neerakkal, Sujeeth and Minkov, Ivan and Hille, Jacques and Temanni, Mohamed-Ramzi and Marriott, Andrew S. and Bergstr{\"o}m, Ed and Thomas-Oates, Jane and Antonio, Carla and M{\"u}ller-R{\"o}ber, Bernd and Schippers, Jos H. M. and Fernie, Alisdair R. and Toneva, Valentina},
  title     = {Molecular mechanisms of desiccation tolerance in the resurrection glacial relic Haberlea rhodopensis},
  series = {Cellular and molecular life sciences},
  volume    = {70},
  journal   = {Cellular and molecular life sciences},
  number    = {4},
  publisher = {Springer},
  address   = {Basel},
  issn      = {1420-682X},
  doi       = {10.1007/s00018-012-1155-6},
  pages     = {689 -- 709},
  year      = {2013},
  abstract  = {Haberlea rhodopensis is a resurrection plant with remarkable tolerance to desiccation. Haberlea exposed to drought stress, desiccation, and subsequent rehydration showed no signs of damage or severe oxidative stress compared to untreated control plants. Transcriptome analysis by next-generation sequencing revealed a drought-induced reprogramming, which redirected resources from growth towards cell protection. Repression of photosynthetic and growth-related genes during water deficiency was concomitant with induction of transcription factors (members of the NAC, NF-YA, MADS box, HSF, GRAS, and WRKY families) presumably acting as master switches of the genetic reprogramming, as well as with an upregulation of genes related to sugar metabolism, signaling, and genes encoding early light-inducible (ELIP), late embryogenesis abundant (LEA), and heat shock (HSP) proteins. At the same time, genes encoding other LEA, HSP, and stress protective proteins were constitutively expressed at high levels even in unstressed controls. Genes normally involved in tolerance to salinity, chilling, and pathogens were also highly induced, suggesting a possible cross-tolerance against a number of abiotic and biotic stress factors. A notable percentage of the genes highly regulated in dehydration and subsequent rehydration were novel, with no sequence homology to genes from other plant genomes. Additionally, an extensive antioxidant gene network was identified with several gene families possessing a greater number of antioxidant genes than most other species with sequenced genomes. Two of the transcripts most abundant during all conditions encoded catalases and five more catalases were induced in water-deficient samples. Using the pharmacological inhibitor 3-aminotriazole (AT) to compromise catalase activity resulted in increased sensitivity to desiccation. Metabolome analysis by GC or LC-MS revealed accumulation of sucrose, verbascose, spermidine, and gamma-aminobutyric acid during drought, as well as particular secondary metabolites accumulating during rehydration. This observation, together with the complex antioxidant system and the constitutive expression of stress protective genes suggests that both constitutive and inducible mechanisms contribute to the extreme desiccation tolerance of H. rhodopensis.},
  language  = {en}
}
@article{GliwickaNowakBalazadehetal.2013,
  author    = {Gliwicka, Marta and Nowak, Katarzyna and Balazadeh, Salma and M{\"u}ller-R{\"o}ber, Bernd and Gaj, Malgorzata D.},
  title     = {Extensive Modulation of the Transcription Factor Transcriptome during Somatic Embryogenesis in Arabidopsis thaliana},
  series = {PLoS one},
  volume    = {8},
  journal   = {PLoS one},
  number    = {7},
  publisher = {PLoS},
  address   = {San Fransisco},
  issn      = {1932-6203},
  doi       = {10.1371/journal.pone.0069261},
  pages     = {20},
  year      = {2013},
  abstract  = {Molecular mechanisms controlling plant totipotency are largely unknown and studies on somatic embryogenesis (SE), the process through which already differentiated cells reverse their developmental program and become embryogenic, provide a unique means for deciphering molecular mechanisms controlling developmental plasticity of somatic cells. Among various factors essential for embryogenic transition of somatic cells transcription factors (TFs), crucial regulators of genetic programs, are believed to play a central role. Herein, we used quantitative real-time polymerase chain reaction (qRT-PCR) to identify TF genes affected during SE induced by in vitro culture in Arabidopsis thaliana. Expression profiles of 1,880 TFs were evaluated in the highly embryogenic Col-0 accession and the non-embryogenic tanmei/emb2757 mutant. Our study revealed 729 TFs whose expression changes during the 10-days incubation period of SE; 141 TFs displayed distinct differences in expression patterns in embryogenic versus non-embryogenic cultures. The embryo-induction stage of SE occurring during the first 5 days of culture was associated with a robust and dramatic change of the TF transcriptome characterized by the drastic up-regulation of the expression of a great majority (over 80\%) of the TFs active during embryogenic culture. In contrast to SE induction, the advanced stage of embryo formation showed attenuation and stabilization of transcript levels of many TFs. In total, 519 of the SE-modulated TFs were functionally annotated and transcripts related with plant development, phytohormones and stress responses were found to be most abundant. The involvement of selected TFs in SE was verified using T-DNA insertion lines and a significantly reduced embryogenic response was found for the majority of them. This study provides comprehensive data focused on the expression of TF genes during SE and suggests directions for further research on functional genomics of SE.},
  language  = {en}
}
@article{LukoszekMuellerRoeberIgnatova2013,
  author    = {Lukoszek, Radoslaw and M{\"u}ller-R{\"o}ber, Bernd and Ignatova, Zoya},
  title     = {Interplay between polymerase II- and polymerase III-assisted expression of overlapping genes},
  series = {FEBS letters : the journal for rapid publication of short reports in molecular biosciences},
  volume    = {587},
  journal   = {FEBS letters : the journal for rapid publication of short reports in molecular biosciences},
  number    = {22},
  publisher = {Elsevier},
  address   = {Amsterdam},
  issn      = {0014-5793},
  doi       = {10.1016/j.febslet.2013.09.033},
  pages     = {3692 -- 3695},
  year      = {2013},
  abstract  = {Up to 15\% of the genes in different genomes overlap. This architecture, although beneficial for the genome size, represents an obstacle for simultaneous transcription of both genes. Here we analyze the interference between RNA-polymerase II (Pol II) and RNA-polymerase III (Pol III) when transcribing their target genes encoded on opposing strands within the same DNA fragment in Arabidopsis thaliana. The expression of a Pol II-dependent protein-coding gene negatively correlated with the transcription of a Pol III-dependent, tRNA-coding gene set. We suggest that the architecture of the overlapping genes introduces an additional layer of control of gene expression. (C) 2013 Federation of European Biochemical Societies. Published by Elsevier B.V. All rights reserved.},
  language  = {en}
}
@article{MatallanaRamirezRaufFarageBarhometal.2013,
  author    = {Matallana-Ramirez, Lilian P. and Rauf, Mamoona and Farage-Barhom, Sarit and Dortay, Hakan and Xue, Gang-Ping and Droege-Laser, Wolfgang and Lers, Amnon and Balazadeh, Salma and M{\"u}ller-R{\"o}ber, Bernd},
  title     = {NAC Transcription Factor ORE1 and Senescence-Induced BIFUNCTIONAL NUCLEASE1 (BFN1) Constitute a Regulatory Cascade in Arabidopsis},
  series = {Molecular plant},
  volume    = {6},
  journal   = {Molecular plant},
  number    = {5},
  publisher = {Oxford Univ. Press},
  address   = {Oxford},
  issn      = {1674-2052},
  doi       = {10.1093/mp/sst012},
  pages     = {1438 -- 1452},
  year      = {2013},
  abstract  = {The NAC transcription factor ORE1 is a key regulator of senescence in Arabidopsis thaliana. Here, we demonstrate that senescence-induced and cell death-associated BIFUNCTIONAL NUCLEASE1 (BFN1) is a direct downstream target of ORE1, revealing a previously unknown regulatory cascade.Senescence is a highly regulated process that involves the action of a large number of transcription factors. The NAC transcription factor ORE1 (ANAC092) has recently been shown to play a critical role in positively controlling senescence in Arabidopsis thaliana; however, no direct target gene through which it exerts its molecular function has been identified previously. Here, we report that BIFUNCTIONAL NUCLEASE1 (BFN1), a well-known senescence-enhanced gene, is directly regulated by ORE1. We detected elevated expression of BFN1 already 2 h after induction of ORE1 in estradiol-inducible ORE1 overexpression lines and 6 h after transfection of Arabidopsis mesophyll cell protoplasts with a 35S:ORE1 construct. ORE1 and BFN1 expression patterns largely overlap, as shown by promoterreporter gene (GUS) fusions, while BFN1 expression in senescent leaves and the abscission zones of maturing flower organs was virtually absent in ore1 mutant background. In vitro binding site assays revealed a bipartite ORE1 binding site, similar to that of ORS1, a paralog of ORE1. A bipartite ORE1 binding site was identified in the BFN1 promoter; mutating the cis-element within the context of the full-length BFN1 promoter drastically reduced ORE1-mediated transactivation capacity in transiently transfected Arabidopsis mesophyll cell protoplasts. Furthermore, chromatin immunoprecipitation (ChIP) demonstrates in vivo binding of ORE1 to the BFN1 promoter. We also demonstrate binding of ORE1 in vivo to the promoters of two other senescence-associated genes, namely SAG29/SWEET15 and SINA1, supporting the central role of ORE1 during senescence.},
  language  = {en}
}
@article{MehrniaBalazadehZanoretal.2013,
  author    = {Mehrnia, Mohammad and Balazadeh, Salma and Zanor, Maria-Ines and M{\"u}ller-R{\"o}ber, Bernd},
  title     = {EBE, an AP2/ERF transcription factor highly expressed in proliferating cells, affects shoot architecture in arabidopsis},
  series = {Plant physiology : an international journal devoted to physiology, biochemistry, cellular and molecular biology, biophysics and environmental biology of plants},
  volume    = {162},
  journal   = {Plant physiology : an international journal devoted to physiology, biochemistry, cellular and molecular biology, biophysics and environmental biology of plants},
  number    = {2},
  publisher = {American Society of Plant Physiologists},
  address   = {Rockville},
  issn      = {0032-0889},
  doi       = {10.1104/pp.113.214049},
  pages     = {842 -- 857},
  year      = {2013},
  abstract  = {We report about ERF BUD ENHANCER (EBE; At5g61890), a transcription factor that affects cell proliferation as well as axillary bud outgrowth and shoot branching in Arabidopsis (Arabidopsis thaliana). EBE encodes a member of the APETALA2/ETHYLENE RESPONSE FACTOR (AP2/ERF) transcription factor superfamily; the gene is strongly expressed in proliferating cells and is rapidly and transiently up-regulated in axillary meristems upon main stem decapitation. Overexpression of EBE promotes cell proliferation in growing calli, while the opposite is observed in EBE-RNAi lines. EBE overexpression also stimulates axillary bud formation and outgrowth, while repressing it results in inhibition of bud growth. Global transcriptome analysis of estradiol-inducible EBE overexpression lines revealed 48 EBE early-responsive genes, of which 14 were up-regulated and 34 were downregulated. EBE activates several genes involved in cell cycle regulation and dormancy breaking, including D-type cyclin CYCD3; 3, transcription regulator DPa, and BRCA1-ASSOCIATED RING DOMAIN1. Among the down-regulated genes were DORMANCY-ASSOCIATED PROTEIN1 (AtDRM1), AtDRM1 homolog, MEDIATOR OF ABA-REGULATED DORMANCY1, and ZINC FINGER HOMEODOMAIN5. Our data indicate that the effect of EBE on shoot branching likely results from an activation of genes involved in cell cycle regulation and dormancy breaking.},
  language  = {en}
}
@article{NguyenSchippersGoniRamosetal.2013,
  author    = {Nguyen, Hung M. and Schippers, Jos H. M. and Goni-Ramos, Oscar and Christoph, Mathias P. and Dortay, Hakan and van der Hoorn, Renier A. L. and M{\"u}ller-R{\"o}ber, Bernd},
  title     = {An upstream regulator of the 26S proteasome modulates organ size in Arabidopsis thaliana},
  series = {The plant journal},
  volume    = {74},
  journal   = {The plant journal},
  number    = {1},
  publisher = {Wiley-Blackwell},
  address   = {Hoboken},
  issn      = {0960-7412},
  doi       = {10.1111/tpj.12097},
  pages     = {25 -- 36},
  year      = {2013},
  abstract  = {In both animal and plant kingdoms, body size is a fundamental but still poorly understood attribute of biological systems. Here we report that the Arabidopsis NAC transcription factor Regulator of Proteasomal Gene Expression' (RPX) controls leaf size by positively modulating proteasome activity. We further show that the cis-element recognized by RPX is evolutionarily conserved between higher plant species. Upon over-expression of RPX, plants exhibit reduced growth, which may be reversed by a low concentration of the pharmacological proteasome inhibitor MG132. These data suggest that the rate of protein turnover during growth is a critical parameter for determining final organ size.},
  language  = {en}
}
@article{OmranianKlieMuellerRoeberetal.2013,
  author    = {Omranian, Nooshin and Klie, Sebastian and M{\"u}ller-R{\"o}ber, Bernd and Nikoloski, Zoran},
  title     = {Network-based segmentation of biological multivariate time series},
  series = {PLoS one},
  volume    = {8},
  journal   = {PLoS one},
  number    = {5},
  publisher = {PLoS},
  address   = {San Fransisco},
  issn      = {1932-6203},
  doi       = {10.1371/journal.pone.0062974},
  pages     = {10},
  year      = {2013},
  abstract  = {Molecular phenotyping technologies (e.g., transcriptomics, proteomics, and metabolomics) offer the possibility to simultaneously obtain multivariate time series (MTS) data from different levels of information processing and metabolic conversions in biological systems. As a result, MTS data capture the dynamics of biochemical processes and components whose couplings may involve different scales and exhibit temporal changes. Therefore, it is important to develop methods for determining the time segments in MTS data, which may correspond to critical biochemical events reflected in the coupling of the system's components. Here we provide a novel network-based formalization of the MTS segmentation problem based on temporal dependencies and the covariance structure of the data. We demonstrate that the problem of partitioning MTS data into k segments to maximize a distance function, operating on polynomially computable network properties, often used in analysis of biological network, can be efficiently solved. To enable biological interpretation, we also propose a breakpoint-penalty (BP-penalty) formulation for determining MTS segmentation which combines a distance function with the number/length of segments. Our empirical analyses of synthetic benchmark data as well as time-resolved transcriptomics data from the metabolic and cell cycles of Saccharomyces cerevisiae demonstrate that the proposed method accurately infers the phases in the temporal compartmentalization of biological processes. In addition, through comparison on the same data sets, we show that the results from the proposed formalization of the MTS segmentation problem match biological knowledge and provide more rigorous statistical support in comparison to the contending state-of-the-art methods.},
  language  = {en}
}
@article{PetrovSchippersBeninaetal.2013,
  author    = {Petrov, Veselin and Schippers, Jos and Benina, Maria and Minkov, Ivan and M{\"u}ller-R{\"o}ber, Bernd and Gechev, Tsanko S.},
  title     = {In search for new players of the oxidative stress network by phenotyping an Arabidopsis T-DNA mutant collection on reactive oxygen species-eliciting chemicals},
  series = {Plant omics},
  volume    = {6},
  journal   = {Plant omics},
  number    = {1},
  publisher = {Southern Cross Publ.},
  address   = {Lismore},
  issn      = {1836-0661},
  pages     = {46 -- 54},
  year      = {2013},
  abstract  = {The ability of some chemical compounds to cause oxidative stress offers a fast and convenient way to study the responses of plants to reactive oxygen species (ROS). In order to unveil potential novel genetic players of the ROS-regulatory network, a population of similar to 2,000 randomly selected Arabidopsis thaliana T-DNA insertion mutants was screened for ROS sensitivity/resistance by growing seedlings on agar medium supplemented with stress-inducing concentrations of the superoxide-eliciting herbicide methyl viologen or the catalase inhibitor 3-amino-triazole. A semi-robotic setup was used to capture and analyze images of the chemically treated seedlings which helped interpret the screening results by providing quantitative information on seedling area and healthy-to-chlorotic tissue ratios for data verification. A ROS-related phenotype was confirmed in three of the initially selected 33 mutant candidates, which carry T-DNA insertions in genes encoding a Ring/Ubox superfamily protein, ABI5 binding protein 1 (AFP1), previously reported to be involved in ABA signaling, and a protein of unknown function, respectively. In addition, we identified six mutants, most of which have not been described yet, that are related to growth or chloroplast development and show defects in a ROS-independent manner. Thus, semi-automated image capturing and phenotyping applied on publically available T-DNA insertion collections adds a simple means for discovering novel mutants in complex physiological processes and identifying the genes involved.},
  language  = {en}
}
@article{RaufArifDortayetal.2013,
  author    = {Rauf, Mamoona and Arif, Muhammad and Dortay, Hakan and Matallana-Ramirez, Lilian P. and Waters, Mark T. and Nam, Hong Gil and Lim, Pyung-Ok and M{\"u}ller-R{\"o}ber, Bernd and Balazadeh, Salma},
  title     = {ORE1 balances leaf senescence against maintenance by antagonizing G2-like-mediated transcription},
  series = {EMBO reports},
  volume    = {14},
  journal   = {EMBO reports},
  number    = {4},
  publisher = {Nature Publ. Group},
  address   = {London},
  issn      = {1469-221X},
  doi       = {10.1038/embor.2013.24},
  pages     = {382 -- 388},
  year      = {2013},
  abstract  = {Leaf senescence is a key physiological process in all plants. Its onset is tightly controlled by transcription factors, of which NAC factor ORE1 (ANAC092) is crucial in Arabidopsis thaliana. Enhanced expression of ORE1 triggers early senescence by controlling a downstream gene network that includes various senescence-associated genes. Here, we report that unexpectedly ORE1 interacts with the G2-like transcription factors GLK1 and GLK2, which are important for chloroplast development and maintenance, and thereby for leaf maintenance. ORE1 antagonizes GLK transcriptional activity, shifting the balance from chloroplast maintenance towards deterioration. Our finding identifies a new mechanism important for the control of senescence by ORE1.},
  language  = {en}
}
@article{RaufArifFisahnetal.2013,
  author    = {Rauf, Mamoona and Arif, Muhammad and Fisahn, Joachim and Xue, Gang-Ping and Balazadeh, Salma and M{\"u}ller-R{\"o}ber, Bernd},
  title     = {NAC transcription factor speedy hyponastic growth regulates flooding-induced leaf movement in arabidopsis},
  series = {The plant cell},
  volume    = {25},
  journal   = {The plant cell},
  number    = {12},
  publisher = {American Society of Plant Physiologists},
  address   = {Rockville},
  issn      = {1040-4651},
  doi       = {10.1105/tpc.113.117861},
  pages     = {4941 -- 4955},
  year      = {2013},
  abstract  = {In rosette plants, root flooding (waterlogging) triggers rapid upward (hyponastic) leaf movement representing an important architectural stress response that critically determines plant performance in natural habitats. The directional growth is based on localized longitudinal cell expansion at the lower (abaxial) side of the leaf petiole and involves the volatile phytohormone ethylene (ET). We report the existence of a transcriptional core unit underlying directional petiole growth in Arabidopsis thaliana, governed by the NAC transcription factor SPEEDY HYPONASTIC GROWTH (SHYG). Overexpression of SHYG in transgenic Arabidopsis thaliana enhances waterlogging-triggered hyponastic leaf movement and cell expansion in abaxial cells of the basal petiole region, while both responses are largely diminished in shyg knockout mutants. Expression of several EXPANSIN and XYLOGLUCAN ENDOTRANSGLYCOSYLASE/HYDROLASE genes encoding cell wall-loosening proteins was enhanced in SHYG overexpressors but lowered in shyg. We identified ACC OXIDASE5 (ACO5), encoding a key enzyme of ET biosynthesis, as a direct transcriptional output gene of SHYG and found a significantly reduced leaf movement in response to root flooding in aco5 T-DNA insertion mutants. Expression of SHYG in shoot tissue is triggered by root flooding and treatment with ET, constituting an intrinsic ET-SHYG-ACO5 activator loop for rapid petiole cell expansion upon waterlogging.},
  language  = {en}
}